Alternative splicing of VWFA modules generates variants of type VI collagen α3 chain with a distinctive expression pattern in embryonic chicken tissues and potentially different adhesive function

Matrix Biology

Volumn 16, Issue 7, 1998, Pages 427-442

  Doliana, Roberto ^a   Mucignat, Maria Teresa ^a   Segat, Daniela ^a   Zanussi, Stefania ^a   Fabbro, Carla ^a   Lakshmi, T R M ^a,c   Colombatti, Alfonso ^a,b  

^a CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^b UNIVERSITY OF UDINE   (Italy)

^c Ctr for Clin and Research Training   (Italy)

Author keywords

Alternative splicing; Cell adhesion; Tissue variants; Type VI collagen

Indexed keywords

ANTIBODY; CELL ADHESION MOLECULE; COLLAGEN TYPE 6; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; AVIAN STOMACH; CELL ADHESION; CHICK EMBRYO; CONTROLLED STUDY; DENSITOMETRY; EMBRYO; EXON; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN VARIANT; SKELETAL MUSCLE; SKIN; TISSUE DISTRIBUTION;

ANIMALIA; AVES; GALLUS GALLUS;

EID: 0031953180     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0945-053X(98)90015-4     Document Type: Article

References (54)

1. Ayad, S.A., Marriott, A., Morgan, K. and Grant M.E.: Bovine cartilage types VI and IX collagens. Biochem. J. 262: 753-761, 1989
2. Aumailley, M., Mann, K., von der Mark, H. and Timpl, R.: Cell attachment properties of collagen type VI and Arg-Gly-Asp dependent binding to its α2 (VI) and α3(VI) chains. Exp. Cell Res. 181: 463-474, 1989
3. Bearz, A., Tolazzi, G., Leonardi, A., Pucillo, C., Tell, G., Colombatti, A. and Formisano, S.: Expression, purification and functional characterization of a Kunitz-type module from chicken type VI collagen. Biochem. Biophys. Res. Commun. 215: 1050-1055, 1995.
4. Bidanset, D.J., Guidry, C., Rosenberg, L.C., Choi, H.U., Timpl, R. and Hook, M.: Binding of the proteoglycan decorin to collagen type VI. J. Biol. Chem. 267: 5250-5256, 1992.
5. Bonaldo, P. and Colombatti, A.: The C-terminus of the chicken α3 collagen VI is a unique mosaic structure with GPIb-like, fibronectin type III and Kunitz modules. J. Biol. Chem. 264: 20235-20239, 1989.
6. Bonaldo, P., Russo, V., Bucciotti, P., Bressan, G.M. and Colombatti A.: α1 chain of chick type VI collagen. cDNA sequence reveals a hybrid molecule made of one short collagen and three von Willebrand factor type A like domains. J. Biol. Chem. 264: 5575-5580, 1989.
7. Bonaldo P., Russo, V., Bucciotti, R, Doliana, R. and Colombatti, A.: Structural and functional features of the α3 chain indicate a bridging role for chicken collagen type VI in connective tissues. Biochemistry 29: 1245-1254, 1990.
8. Bork, P. and Koonin, E.V. Protein sequence motifs. Curr. Opin. Struct. Biol. 6: 366-375, 1996.
9. Bressan, G.M., Argos, P. and Stanley, K.K.: Repeating structure of chick tropoelastin revealed by complementary DNA cloning. Biochemistry 26: 1497-1503, 1987.
10. Bruns, R., Press, W., Engvall, E., Timpl, R. and Gross, J.: Type VI collagen in extracellular, 100-nm periodic filaments and fibrils: identification by immunoelectron microscopy. J. Cell Biol. 103: 393-404, 1986.
11. Chomczynski, P. and Sacchi, N.: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-choloroform extraction. Anal. Biochem. 162: 156-159, 1987.
12. Chu, M-L., Pan, T-C., Conway, D., Kuo, H-J., Glanville, R.W., Timpl, R., Mann, K. and Deutzmann, R.: Sequence analysis of α1(VI) and α2(VI) chains of human type VI collagen reveals internal triplication of globular domains similar to the A domains of vWF and two α2(VI) chain variants that differ in the carboxyl terminus. EMBO J. 8: 1939-1946, 1989.
13. Chu, M.-L., Zhang, R.-Z., Pan, T., Stokes, D., Conway, D., Kuo, H.-J., Glanville, R., Mayer, U., Mann, K., Deutzmann, R. and Timpl, R.: Mosaic structure of globular domains in the human type VI collagen α3 chain: similarity to von Willebrand Factor, fibronectin, actin, salivary proteins and aprotonin type protease inhibitors. EMBO J. 9: 385-393, 1990.
14. Colombatti A., Ainger, K. and Colizzi, F.: Type VI collagen: High yields of a molecule with multiple forms of α3 chain from avian and human tissues. Matrix 9: 177-184, 1989.
15. Colombatti A., Ainger K., Mucignat M.-T. and Bonaldo P.: Monoclonal antibodies for the different chains of chick type VI collagen. Collagen Rel. Res. 8: 33 1-337, 1988.
16. Colombatti A. and Bonaldo P.: Biosynthesis of chick type VI collagen. II. Processing and secretion in fibroblasts and smooth muscle cells. J. Biol. Chem. 262: 14461-4466, 1987.
17. Colombatti, A., Bonaldo P., Ainger, K., Bressan, G.M. and Volpin, D.: Biosynthesis of chick type VI collagen. I. Intracellular assembly and molecular structure. J. Biol. Chem. 262: 14454-14460, 1987.
18. Colombatti A., Bonaldo P. and Doliana R.: Type A modules: Interacting domains found in several non-fibrillar collagens and in other extracellular matrix proteins. Matrix 13: 297-306, 1993.
19. Doane, K.J., Yang, G. and Birk, D.E.: Corneal cell-matrix interactions: type VI collagen promotes adhesion and spreading of corneal fibroblasts. Exp. Cell Res. 200: 490-499, 1992.
20. Doliana, R., Bonaldo, P. and Colombatti, A.: Multiple forms of chicken α3(VI) collagen chain generated by alternative splicing in type A repeat domains. J. Cell Biol. 111: 2197-2205, 1990.
21. Dziadek, M., Darling, P., Bakker, M., Overall, M., Zhang, R.-Z., Pan, T.-C., Tillet, E., Timpl, R. and Chu, M.-L.: Deposition of collagen in the extracellular matrix during mouse embryogenesis correlates with expression of the α3(VI) subunit gene. Exp. Cell Res. 226: 302-315, 1996.
22. Engel, J., Furthmayr, H., Odermatt, E., von der Mark, H., Aumailley, M., Fleischmajer, R. and Timpl, R.: Structure and macromolecular organization of type VI collagen. Ann. N.Y. Acad. Sci. 460: 25-37, 1985.
23. Engvall, E., Hessle, H. and Klier, G.: Molecular assembly, secretion and matrix deposition of type VI collagen. J. Cell Biol. 102: 703-710, 1986.
24. Fleischmajer, R., Perlish, J.S. and Faraggiana, T.: Rotary shadowing of collagen monomers, oligomers, and fibrils during tendon fibrillogenesis. J. Histochem. Cytochem. 39: 51-58, 1991.
25. ffrench-Constant, C.: Alternative splicing of fibronectin. Many different proteins but few different functions. Exp. Cell Res. 221: 261-271, 1995.
26. ffrench-Constant, C. and Hynes, R.O.: Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo. Development 106: 375-388, 1989.
27. Furthmayr, H., Wiedemann, H., Timpl, R., Odermatt, E. and Engel, J. Electronmicroscopical approach to a structural model of intima collagen. Biochem. J. 211: 303-311, 1983.
28. Gentili, C., Doliana, R., Bet, P., Campanile, G., Colombatti, A., Descalzi Cancedda, F. and Cancedda, R.: Ovotransferrin and ovotransferrin receptor expression during chondrogenesis and endochondral bone formation in developing chick embryo. J. Cell Biol. 124: 579-588, 1994.
29. Hatamochi, A., Aumailley, M. and Mauch, C.: Regulation of collagen VI expression in fibroblasts. Effects of cell density, cell-matrix interactions, and chemical transformation. J. Biol. Chem. 264: 3494-3499, 1989.
30. Heckmann, M., Aumailley, M., Chu, M.-L., Timpl, R. and Krieg, T.: Effect of transforming growth factor-β on collagen type VI expression in human dermal fibroblasts. FEBS Lett. 310: 79-82, 1992.
31. Jander, R., Troyer, D. and Rauterberg, J.: A collagen-like glycoprotein of the extracellular matrix is the undegraded form of type VI collagen. Biochemistry 23: 3675-3681, 1984.
32. Keene, D.R., Engvall, E. and Glanville, R.W.: Ultrastructure of type VI collagen in human skin and cartilage suggests an anchoring function for this filamentous network. J. Cell Biol. 107: 1995-2006, 1988.
33. Kielty, C.M., Boot-Handford, R.P., Ayad, S., Shuttleworth, C.H. and Grant, M.: Molecular composition of type VI collagen. Evidence for chain heterogeneity in mammalian tissues and cultured cells. Biochem. J. 272: 787-795, 1990.
34. Kielty, C.M., Whittaker, S.P., Grant, M.E. and Shuttleworth, C.A.: Type VI collagen microfibrils: evidence for a structural association with hyaluronan. J. Cell Biol. 118: 979-990, 1992.
35. Klein, G., Muller, CA., Tillet, E., Chu, M.-L. and Timpl, R.: Collagen type VI in the human bone marrow microenvironment: a strong cytoadhesive component. Blood 86: 1740-1748, 1995.
36. Koller, E., Winterhalter, K.H. and Trueb, B.: The globular domains of type VI collagen are related to the collagen-binding domains of cartilage matrix protein and von Willebrand factor. EMBO J. 8: 1073-1077, 1989.
37. Kuo, H.-J., Keene, D.R. and Glanville, R.W.: Orientation of type VI collagen monomers in molecular aggregates. Biochemistry 28: 3757-3762, 1989.
38. Kuo H-J, Keene D and Glanville, R.W.: The macromolecular structure of type-VI collagen. Formation and stability of filaments. Eur. J. Biochem. 232: 364-372, 1995.
39. Lotz, M.M., Burdsal, C.A., Erickson, H.P. and McClay, D.R.: Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response. J. Cell Biol. 109: 1795-1805, 1989.
40. Markmeyer, P., Ruhlmann, A., Englisch, U. and Cramer F.: The pAX plasmids: a new gene-fusion vector for sequencing, mutagenesis and expression of proteins in Escherichia coli. Gene 93: 129-134, 1990.
41. Mayer, U., Poeschl, E., Nischt, R., Specks, U., Pan, T.-C., Chu, M.-L. and Timpl, R.: Recombinant expression and properties of the Kunitz-type protease-inhibitor module from human type VI collagen α3(VI) chain. Eur. J. Biochem. 225: 573-580, 1994.
42. McDevitt, C.A., Marcelino, J. and Tucker, L.: Interaction of intact type VI collagen with hyaluronan. FEBS Lett. 294: 167-170, 1991.
43. Nishiyama, A. and Stallcup, W.B.: Expression of NG2 proteoglycan causes retention of type VI collagen on the cell surface. Mol. Biol. Cell 4: 1097-1108, 1993.
44. Perris, R., Kuo, H.J., Glanville, R.W., Leibold, S. and Bronner-Fraser, M.: Neural crest cell interaction with type VI collagen is mediated by multiple cooperative binding sites within triple-helix and globular domains. Exp. Cell Res. 209: 103-117, 1993.
45. Pfaff, M., Aumailley, M., Specks, U., Knolle, J., Zerwes, H.G. and Timpl, R.: Integrin and Arg-Gly-Asp dependence of cell adhesion to the native and unfolded triple helix of collagen type VI. Exp. Cell Res. 206: 167-176, 1993.
46. Segat, D., Pucillo, C., Marotta, G., Perris, R. and Colombatti, A.: Differential attachment of human neoplastic B cells to purified extracellular matrix molecules. Blood 83: 1586-1594, 1994.
47. Specks, U., Mayer, U. and Nitsch, R.: Structure of recombinant N-terminal globule of type VI collagen α3 chain and its binding to heparin and hyaluronan. EMBO J. 11: 4281-4290, 1992.
48. Stempfer, G., Holl-Neugebauer, B. and Rudolph, R.: Improved refolding of an immobilized fusion protein. Nat. Biotech. 14: 329-334, 1996.
49. Stokes, D.G., Saitta, B., Timpl, R. and Chu, M.-L.: Human α3(VI) collagen gene. Characterization of exons coding for the amino-terminal globular domain and alternative splicing in normal and tumor cells. J. Biol. Chem. 266: 8626-8633, 1991.
50. Timpl, R. and Chu M-L. Microfibrillar collagen type VI. In: Extracellular Matrix Assembly and Structure, ed. by Yurchenco, P.D., Birk D.E. and Mecham, R.P., Academic Press, San Diego, 1994, pp 207-234.
51. von der Mark, H., Aumailley, M., Wick, G., Fleischmajer, R. and Timpl, R.: Immunohistochemistry, genuine size and tissue localization of collagen VI. Eur. J. Biochem. 142: 493-502, 1984.
52. Wayner, E.A. and Carter, W.G.: Identification of multiple cell adhesion receptors for type VI collagen and fibronectin in human fibrosarcoma cells possessing unique a and common bsubunits. J. Cell Biol. 105: 1873-1884, 1987.
53. Wu, J.-J., Eyre, D.R. and Slayter, H.S.: Type VI collagen of the invertebral disc. Biochemical and electron-microscopic characterization of the native protein. Biochem. J. 248; 373-381, 1987.
54. Zanussi, S., Doliana, R., Segat, D., Bonaldo, P. and Colombatti, A.: The human type VI collagen gene. J. Biol. Chem. 267: 24082-24089, 1992.